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J Appl Physiol 82: 1024, 1997;
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Journal of Applied Physiology
Vol. 82, No. 3, pp. 1024-1024, March 1997
METABOLISM

SPECIAL COMMUNICATION

High-energy phosphates and tension production in rabbit tibialis anterior/extensor digitorum longus muscles

T. W. Ryschon1, J. C. Jarvis2, S. Salmons2, and R. S. Balaban1

1 Laboratory of Cardiac Energetics, National Heart, Lung, and Blood Institute, Bethesda, Maryland 20892; and 2 Department of Human Anatomy and Cell Biology, University of Liverpool, Liverpool L69 3BX, United Kingdom

ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES

ABSTRACT

Ryschon, T. W., J. C. Jarvis, S. Salmons, and R. S. Balaban. High-energy phosphates and tension production in rabbit tibialis anterior/extensor digitorum longus muscles. J. Appl. Physiol. 82(3): 1024-1029, 1997.---The effects of repetitive muscle contraction on energy state and tension production were studied in rabbit tibialis anterior/extensor digitorum longus muscles that had been subjected to 90 days of continuous indirect electrical stimulation at 10 Hz. Anesthetized chronically stimulated and control rabbits were challenged with 15 min of stimulation at 4 and 15 tetani/min. Pi-to-phosphocreatine (PCr) ratio (Pi/PCr) was measured in vivo before, during, and after acute stimulation by 31P-magnetic resonance spectroscopy, and tension was recorded at the same time. Although Pi/PCr was low at rest, it was significantly higher in chronically stimulated muscle than in control muscle (0.20 ± 0.02 vs. 0.05 ± 0.01, P < 0.05). Stimulation of control muscle for 15 min at both 4 and 15 tetani/min induced a significant rise in Pi/PCr, whereas the same conditions in chronically stimulated muscle did not produce any significant departure from initial levels. The tension produced by control muscle fell to 93 ± 3% of its initial value during stimulation at 4 tetani/min and to 61 ± 7% at 15 tetani/min, respectively. In chronically stimulated muscle, on the other hand, tension was potentiated above its initial level at both stimulation rates (135 ± 15 and 138 ± 11%, respectively) and remained significantly elevated throughout each trial. The ability of chronically stimulated muscle to sustain high levels of activity with minimal perturbations in Pi/PCr or decrement in tension is attributable to cellular adaptations that include a well-documented increase in oxidative capacity.

fatigue; chronic stimulation; 31P-magnetic resonance spectroscopy

INTRODUCTION

CHRONIC LOW-FREQUENCY electrical stimulation of the common peroneal nerve of rabbits induces marked alterations in the structure and performance of the tibialis anterior (TA) and extensor digitorum longus (EDL) muscles. During this process there is an increase in oxidative activity, a decrease in anaerobic glycolytic capacity, and a shift toward expression of slow isoforms of myosin; these changes are reflected in a slowing of contraction speed and a marked increase in fatigue resistance (reviewed in Refs. 25 and 27). Although it is known that alterations in muscle protein composition are brought about by changes in mitochondrial gene number (29, 30), transcriptional (14, 16, 30), and posttranslational processes (14, 30), the signaling pathway that links electrical stimulation to gene expression has not been established. If aspects of the response are functionally driven, changes in muscle metabolism with continuous low-frequency stimulation (12, 13, 20) may reveal candidate signaling factors. Changes in the activities of H+, Pi, phosphocreatine (PCr), and ATP, in particular, could provide clues to possible molecular signaling mechanisms as well as insights into the nature of muscle adaptation to exercise.

The primary goal of this study was to develop and to use a system that would permit muscle tension, phosphate metabolites, and pH to be measured simultaneously in vivo during acute electrical stimulation of the TA and EDL muscles of the rabbit. This muscle group was selected for study because much information is already available about the response of its biochemical and contractile characteristics to chronic stimulation (25, 27) and because there is growing interest in this preparation as a model of muscle plasticity (17). To obtain multiple measurements from each limb, 31P-magnetic resonance (MR) spectroscopy was used as a noninvasive means of assessing intramuscular Pi, PCr, and ATP concentrations, as well as pH. Differences in the contractile and metabolic properties of control TA/EDL muscles and TA/EDL muscles that had been subjected to chronic low-frequency stimulation were explored by challenging them with acute tetanic stimulation. This system resembles a previously described model based on chronically stimulated canine latissimus dorsi muscle (6), but in the present study, tension recording and 31P-MR spectroscopy were performed simultaneously, rather than on successive days. The hypothesis was tested that chronic stimulation would induce changes in TA/EDL muscles that increased the stability of ATP metabolites, indexes of muscle free energy, pH, and tension production during acute tetanic stimulation.

METHODS

Animal preparation for chronic stimulation. Adult male New Zealand White rabbits (2.5-3 kg) were housed individually in a climate-controlled room (18-21°C) and were provided with standard laboratory chow ad libitum. Stimulators and electrodes were implanted under aseptic conditions as described previously (12, 15), except that general anesthesia was maintained with 1-3% isoflurane and mechanical ventilation. In each case, stimulation was confined to the anterior compartment of the left hindlimb. Stimulators were activated ~7 days after surgical implantation to allow animals to recover from the stress of surgery. Animal care personnel or the first author of this study palpated the stimulated limb daily to confirm that the implanted device was functioning satisfactorily. The study design called for a chronic stimulation duration of 90 days to induce a uniform adaptation of the EDL muscle, which appears to occur more slowly than in the TA (5, 24). In two of the five rabbits, chronic stimulation was terminated before 90 days, in one case because of stimulator malfunction and in the other because of dry gangrene of a toe on the unstimulated limb. For these reasons, these two rabbits were excluded from further analysis.

Acute stimulation. The acute-stimulation protocol was performed on TA/EDL muscles that had undergone chronic stimulation, and the right TA/EDL muscles of five rabbits that had not undergone surgery. Before acute stimulation, anesthesia was induced with ketamine (50 mg/kg) and acepromazine (0.5 mg/kg im) and was maintained via mechanical ventilation (Siemens-Elema 900D Servo Ventilator, 21-40% O2-balance N2) by using 1-3% isoflurane. A vein and artery from the ear were cannulated for intravenous access and arterial blood pressure and blood gas monitoring, respectively. Dextrose (5% in water) was infused through the ear vein at 6 ml/h to maintain fluid and euglycemia.

The implanted stimulator, inactivated 1.5-2 h earlier, was removed through a small incision in the flank after the implanted leads were freed from the implanted electrodes via an incision over the common peroneal nerve. In an effort to standardize the acute-stimulation technique, a flat, bipolar electrode was sutured under the common peroneal nerve at the level of the fibular head in chronically stimulated and unoperated control limbs. A 3.0-mm hole was drilled through the distal femur to accommodate tapered, nylon pins applied bilaterally to immobilize the limb. Tendons of the TA and EDL muscles were dissected free of underlying connective tissue and clamped together at their resting lengths before being attached to an aluminum load cell (Tedea model 1030, Canoga Park, CA) via a Lexan mortise-tenon style block. All skin incisions were closed, and the animal was placed on a circulating water blanket (38°C) in a Lexan-fiberglass cradle that permitted three-dimensional positioning and immobilization of the lower limb of the rabbit. Muscle length was adjusted for maximal tetanic tension production. The acute-stimulation protocol consisted of a 5-min rest period, 15 min of stimulation at 4 tetani/min (0.7% duty cycle), 20 min of recovery, 15 min of stimulation at 15 tetani/min (2.5% duty cycle), and 15 min of recovery. Metabolic parameters and muscle tension were recorded continuously throughout each experiment. Tetanic contractions were achieved by electrical stimulation of the peroneal nerve (Grass S88 stimulator) with the following parameters: pulse frequency 100 Hz; train duration 100 ms; pulse amplitude 10-20 V (supramaximal); pulse duration 2 ms. Muscle tension above resting tension and arterial blood pressure were recorded on a strip-chart recorder. In all experiments, resting muscle tension was constant for the duration of each experiment. At the completion of each experiment, TA/EDL muscles were excised and weighed.

31P-MR spectroscopy. A rectangular surface coil (31 × 8 mm) tuned to phosphorus (81 MHz) was positioned over the anterolateral lower limb. The cradle was placed in the bore of a superconducting magnet (4.7 Tesla, Oxford Magnetics, Oxford, UK) equipped with Accustar gradients. The magnetic field homogeneity was optimized by manual adjustment of the room temperature shims until PCr line width was <40 Hz. In initial studies, the volume from which data were collected was localized to the TA/EDL group by means of 1H images acquired with a coil of identical dimensions and orientation but tuned to 200 MHz for 1H detection (block size 256 K, sweep width 40 K, field of view 50 mm, repetition time 200 ms, echo time 10 ms). Positioning of the coil relative to these muscles was found to be reproducible by using only external landmarks that were used for subsequent 31P-MR studies. During 31P-MR spectroscopy, the following parameters were used: sweep width 10 kHz, block size 2,048 points, interpulse delay 0.21 s, and a pulse width ranging from 10 to 15 µs (nominal power 1 kW), which was selected to optimize the signal-to-noise ratio (S/N) of the beta -ATP peak, as suggested by Evelhoch et al. (10). The combination of these parameters and 286 scans/spectrum resulted in a 1-min temporal resolution.

Data analysis. One-minute free induction decays were grouped in 5-min signal-averaged blocks before fast Fourier analysis. After line broadening (exponential multiplication of 20 Hz) and baseline correction (GE Omega v. 4.2), the peak areas of Pi and PCr were derived by integration and were not corrected for partial saturation. The Pi/PCr ratio was used as an inverse index of phosphorylation potential. When the S/N for a peak was determined, exponential broadening equal to the half-height peak width was applied (30 Hz for ATP), but other analysis steps were the same. Muscle tension was expressed as grams above resting tension per unit (g) of wet muscle mass (g/g) and as a percentage of initial tetanic tension. Intracellular pH was calculated by using the chemical shift of Pi (23). One-way repeated measures analysis of variance (ANOVA; for normally distributed variables) and the Wilcoxon signed-rank test (for non-normally distributed variables) were used to detect significant changes with time within a rabbit over the course of the experiment. Dunnett's posttest was used to identify significant departures from the initial condition. Group differences among chronically stimulated, unstimulated, and unoperated control muscles were identified by one-way ANOVA for normally distributed variables and by Kruskal-Wallis one-way ANOVA on ranks for variables with non-normal data distributions. Multiple comparisons were conducted by Student-Newman-Keuls and Dunn's method for normally and non-normally distributed variables, respectively. Statistics were computed with the use of SigmaStat v. 1.01 (Jandel Scientific, San Rafael, CA). All values are expressed as means ± SE, and a probability of P < 0.05 was accepted as significant.

RESULTS

Muscle weight. The weight of the TA/EDL muscles in chronically stimulated rabbits (3.4 ± 0.3 g) was significantly less than in unoperated controls (5.3 ± 0.4 g; P < 0.05).

Contractile performance. Tension production for the two groups of rabbits is shown in Fig. 1. Tension production of unoperated control muscle was 258 ± 39 g/g at the onset of 4 tetani/min stimulation and fell slightly during the rest of the stimulation period, reaching 244 ± 37 g/g at 10 min and 241 ± 37 g/g at 15 min of stimulation; however, none of these changes were statistically significant. After 20 min of recovery, tension was 218 ± 31 g/g at the first contraction of 15 tetani/min stimulation. Thereafter, tension decreased to a lower level than during 4 tetani/min, reaching 152 ± 27 g/g at the final contraction (61 ± 7% of initial tension; P < 0.05). In chronically stimulated muscle, tension was potentiated above 84 ± 28 g/g to 105 ± 30 g/g in the first 5 min of stimulation at 4 tetani/min (P < 0.05). After 10 min of stimulation, tension was 107 ± 29 g/g, and it had not increased further by 15 min of stimulation (109 ± 25 g/g). At the onset of 15 tetani/min stimulation, tension was 81 ± 20 g/g and increased significantly (P < 0.05) to 119 ± 16 g/g after 5 min, at which level it stabilized for the rest of the stimulation.
Fig. 1. Tension, normalized to muscle mass (g), in response to stimulation at 4 and 15 tetani/min for chronically stimulated rabbit tibialis anterior (TA)/extensor digitorum longus (EDL; bullet ) muscles and unoperated control muscle (black-triangle). * Significant difference, chronically stimulated vs. unoperated control muscle (P < 0.05).
[View Larger Version of this Image (15K GIF file)]

Metabolic changes. Figure 2 shows spectra from unoperated control and chronically stimulated muscle during acute stimulation at 15 tetani/min. The peaks of Pi, PCr, and ATP are clearly distinguishable in these spectra. The S/N for the beta -phosphate peak of the control spectrum was ~100:1.
Fig. 2. 31P-magnetic resonance (MR) spectra at rest and after 15 min of stimulation at 15 tetani/min and difference spectra for unoperated control (A) and chronically stimulated muscle (B). ppm, Parts/million.
[View Larger Version of this Image (15K GIF file)]

pH. At rest, pH in unoperated control muscle was 7.12 ± 0.02. During 4 and 15 tetani/min stimulation, pH decreased significantly, reaching 7.03 ± 0.04 (P < 0.05) and 6.94 ± 0.03 (P < 0.05) after 15 min of stimulation at 4 and 15 tetani/min, respectively (Fig. 3). At rest, there was no significant difference between the pH of chronically stimulated muscle (7.16 ± 0.02) and that of unoperated control muscle. In chronically stimulated muscle, pH did not change significantly from initial levels during or after stimulation in either trial. Although pH tended to be lower in unoperated control muscles during 4 tetani/min stimulation, the difference relative to chronically stimulated muscle was not significant until the fifth minute of stimulation at 15 tetani/min. At all subsequent time points, pH was significantly lower in unoperated control than in chronically stimulated muscle (Fig. 3).
Fig. 3. Response of muscle pH to stimulation at 4 and 15 tetani/min for chronically stimulated TA/EDL and unoperated control muscle. Symbols are defined as in Fig. 1. * Significant difference, chronically stimulated vs. unoperated control muscle (P < 0.05).
[View Larger Version of this Image (15K GIF file)]

Indexes of phosphorylation potential. Initial values of Pi/PCr were significantly higher for chronically stimulated muscle (0.20 ± 0.02) than for unoperated control muscle (0.05 ± 0.01; P < 0.05). In chronically stimulated muscle, no detectable change took place in Pi/PCr in response to stimulation at either 4 or 15 tetani/min. This behavior differed markedly from that of unoperated control muscle. During stimulation at 4 tetani/min, Pi/PCr increased, reaching 0.26 ± 0.03 at 15 min (Fig. 4). Pi/PCr recovered to initial levels within 15 min (0.05 ± 0.01; P > 0.05). During stimulation at 15 tetani/min, Pi/PCr increased rapidly, reaching 1.68 ± 0.36 at 15 min (P < 0.05 relative to the initial level).
Fig. 4. Response of muscle Pi-to-phosphocreatine (PCr) ratio (Pi/PCr) to stimulation at 4 and 15 tetani/min for chronically stimulated TA/EDL and unoperated control muscle. Symbols are defined as in Fig. 1. * Significant difference, chronically stimulated vs. unoperated control muscle (P < 0.05).
[View Larger Version of this Image (13K GIF file)]

DISCUSSION

In this study, an in vivo model of the rabbit TA/EDL muscle complex was developed in which tension measurement and 31P-MR spectroscopy could be performed simultaneously. The results corroborate previously reported findings on adaptations in fatigue and phosphate metabolism in chronically stimulated muscles (6) and extends them to changes in force, pH, and Pi/PCr occurring dynamically during an acute challenge.

Sampled volume. Axial images obtained with a proton coil of the same dimensions as those used for acquiring 31P-MR spectra indicated that the predominant source of signal in unoperated control muscle was a crescent of muscle extending to one-half the depth of the TA. However, the correspondence between the imaged volume and that sampled spectroscopically would not be precise because of differences in B1 field intensity at 1H and 31P frequencies. Furthermore, chronic stimulation reduced the total muscle mass by 50%, and, because the pulse duration used to acquire the spectra was nearly constant, sampling under these conditions would have extended more deeply into the TA/EDL muscle group. In anticipation of this effect and to minimize any resulting inhomogeneity within the sampled volume, chronic stimulation was carried out for 90 days, a period long enough to ensure complete transformation of all the muscles of the anterior compartment. At the same time, the diameter of the surface coil was deliberately limited to 8 mm, with a view to restricting the sampled volume to this compartment. It is therefore unlikely that the spectroscopic results were influenced to any significant degree by inclusion of unstimulated muscle.

Fatigue resistance. The development of fatigue resistance in fast-twitch skeletal muscle that had been subjected to chronic electrical stimulation was first described 20 years ago (26, 28). The ability of the chronically stimulated, or "conditioned," muscle to maintain a stable tension output during prolonged periods of imposed activity has been confirmed in many subsequent studies in rabbit limb muscles (reviewed in Refs. 25, 27) and in the canine latissimus dorsi muscle (6). Chronically stimulated muscle will eventually show force fatigue but only at work rates very much higher than those that produce fatigue in control muscle (20). Thus, some feature of transformation enables tension to be maintained at contraction rates that normally produce fatigue. Muscle fatigue that occurs in unconditioned muscle during high-intensity contractions of short duration is associated with increases in H+ and lactate (2, 11) and in Pi (3). In chronically stimulated muscle, these metabolic changes are minimal. This can be explained by a tighter coupling between ATP supply and demand such that the by-products of ATP hydrolysis (Pi, H+, ADP) remain at resting levels. The increase in anaerobic glycolysis and the associated increase in proton and lactate production rates that can occur in control muscle are averted, resulting in lower concentrations of the end-products of metabolic activity that are capable of inhibiting force production.

Tetanic tension in control and chronically stimulated muscle. In agreement with previous studies in the rabbit (4, 28), chronically stimulated muscle produced significantly less tetanic tension than unoperated control muscle. Because tetanic tension is closely correlated with muscle cross-sectional area (4), this finding is consistent with the lower total mass of the TA/EDL in these experiments and with the reported observation of smaller fiber cross-sectional areas in muscle transformed by continuous electrical stimulation (27).

Muscle energy state. Muscle phenotype is associated with significant differences in fiber energy state. In vitro biochemical analysis and 31P-MR spectroscopy both show that resting slow-twitch muscle has a lower phosphorylation potential than resting mixed or fast-twitch muscle (23). In the present study, Pi/PCr, an inverse index of phosphorylation potential, was significantly higher in chronically stimulated than in control muscle at rest. This is consistent with the predominantly slow-twitch fiber type composition of chronically stimulated muscle that has been reported previously (25, 27). An alternative explanation that deserves discussion is the possibility of muscle injury associated with stimulation because Pi/PCr is known to increase for several days after damaging eccentric contractions (21). There is, however, good evidence to suggest that injury is not a major consequence of chronic stimulation. In experiments conducted on the same muscles, and under conditions identical to those in the present study, Lexell et al. (19) found histological evidence of degenerating fibers amounting to only 3.5% of TA and 10.4% of EDL muscles by volume, respectively. Moreover, this represented a maximum value, attained at 9 days; after 3 wk of stimulation, no evidence of degenerating fibers could be found (18). Thus the higher resting value of Pi/PCr in chronically stimulated muscle is likely to be the consequence of transformation rather than damage to the fibers.

During tetanic stimulation, Pi/PCr increased in unstimulated control TA/EDL muscle but remained unchanged in chronically stimulated muscle. Similar findings have been reported for the chronically stimulated canine latissimus dorsi muscle (6). The increase in Pi/PCr in unoperated TA/EDL during acute tetanic stimulation is due to PCr hydrolysis, which maintains ATP concentration at constant levels (22), and to Pi accumulation. The stability of Pi/PCr in chronically stimulated muscle indicates that the rate of ATP synthesis was closely coupled to the rate of ATP hydrolysis at both 4 and 15 tetani/min. Thus temporal buffering of ATP concentration was not required. Microscopic examination and in vitro assay of chronically stimulated muscle have demonstrated striking increases in mitochondrial density, oxidative enzyme capacity, and capillarity (9, 12, 25, 27). Thus, chronically stimulated muscle appears to be well equipped to synthesize ATP at the high rates necessary to match the energy requirements of demanding contractions. The close coupling between synthesis of ATP and rates of hydrolysis in chronically stimulated muscle is suggestive of differences between control and chronically stimulated muscle in the fraction of maximum metabolic rate that is required to support tetanic stimulation and/or in the mechanisms that regulate metabolic rate, which might include altered sensitivity to ADP and Pi in vivo (8) or control by NADH (1) or F1-adenosinetriphosphatase activity (7). Studies designed to investigate these possibilities have yet to be performed.

Conclusion. We have shown that it is possible to monitor muscle tension and intramuscular high-energy phosphate compounds simultaneously in an in vivo model. The system was applied to the TA/EDL muscle complex of the rabbit and used to examine contractile and metabolic adaptations to chronic electrical stimulation at 10 Hz. Muscles stimulated for 90 days had undergone a marked reduction in peak tetanic tension and muscle mass from control levels. However, these muscles showed no evidence of fatigue under conditions of acute tetanic stimulation that produced a substantial decline in the force generated by unconditioned muscles in the contralateral limb and in the limbs of unoperated control animals. Despite these demanding conditions, the transformed muscle was able to maintain stable levels of ATP hydrolysis products and a constant Pi/PCr. This increased capacity for homeostasis may be a direct consequence of an increased oxidative capacity, or it may involve changes in the regulation of oxidative phosphorylation. We believe that these results illustrate the potential of this system for studying factors underlying fatigue resistance, regulation of oxidative phosphorylation in skeletal muscle, and metabolic factors that may signal molecular alterations during continuous low-frequency stimulation.

ACKNOWLEDGEMENTS

The authors acknowledge with appreciation the technical assistance of Joni Taylor and Michelle Hastings.

FOOTNOTES

   This work was supported by grants from the Pediatric Scientist Development Program (T. W. Ryschon) and from the British Heart Foundation and Engineering and Physical Sciences Research Council (J. C. Jarvis, S. Salmons).

   Present address for T. W. Ryschon: Chief of Pediatrics, Rosebud Comprehensive Health Care Facility, PO Box 400, Rosebud, SD 57570 (E-mail: ryschon{at}ibm.net).

Received 14 August 1995; accepted in final form 6 September 1996.

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